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Dillenia Indica Fruit Extract Has Glucose and Cholesterol Lowering bioRxiv preprint doi: https://doi.org/10.1101/804815; this version posted October 14, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 1 Dillenia indica fruit extract has Glucose and Cholesterol Lowering 2 effects 3 Shumsuzzaman Khan1,2,4*, Amrita Bhowmik2, SM Badier Rhaman1, Siew 4 Hua Gan4, Begum Rokeya2 5 1Department of Biochemistry & Molecular Biology, Jahangirnagar University, 6 Savar, Dhaka-1342, Bangladesh. 7 2Department of Pharmacology, Biomedical Research Group, Bangladesh 8 Institute of Research and Rehabilitation in Diabetes, Endocrine and 9 Metabolic Disorders (BIRDEM), Dhaka-1000, Bangladesh. 10 3School of Pharmacy, Monash University Malaysia, Jalan Lagoon Selatan, 11 47500 Bandar Sunway, Selangor, Malaysia. 12 13 4Department of Physiology & Biophysics, School of Medicine, Case Western 14 Reserve University, Ohio, USA. 15 16 *Correspondence: [email protected]; Tel.: +14435384402. 17 18 19 20 21 22 23 24 25 Page 1 of 52 bioRxiv preprint doi: https://doi.org/10.1101/804815; this version posted October 14, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 26 Abstract 27 Background: Dillenia indica (D. indica) can suppress carbohydrates 28 hydrolysis by inhibiting α-amylase and α-glucosidase. However, there is a lack 29 of understanding of its therapeutic potential as an antidiabetic and anti- 30 hyperlipidemic agent. 31 Methods and findings: Type 2 diabetes (T2D) was induced by a single 32 intraperitoneal injection of Streptozotocin (STZ; 90mg/kg) and hyperlipidemia 33 by feeding with 1% cholesterol, 5% coconut oil and 5% cow fat diet. 34 Administration of D. indica extracts in water for four weeks triggered a 35 significant (p≤0.05) reduction in fasting serum glucose (FSG) levels with 36 concomitant improvement in serum insulin levels. Both the water- and 37 ethanol-extract of D. indica treated groups showed significant (p≤0.01) 38 reduction in total cholesterol levels by 25% and 19%, respectively. HDL- 39 cholesterol was also augmented (by 14%) in ethanol-extract treated group. 40 Liver glycogen content was higher in the water-extract treated group. 41 Histopathological examination revealed that there was no tubular epithelial 42 cell degeneration or necrosis in the renal tissues or hepatocyte degeneration 43 and sinusoidal dilation in liver tissues in animals that received the water- 44 extract. On the other hand, consumption of D. indica extract with 1% 45 cholesterol, 5% coconut oil diet or with a 5% cow fat diet for 14 days 46 significantly reduced serum cholesterol levels in group-lll (60→45 mg/dl; 47 p≥0.05) and -IV (85→66 mg/dl; p≥0.05) hypercholesterolemic model rats. D. 48 indica fruit extract also reduced serum TG levels (Group-III: 87→65 mg/dl; 49 Group-IV: 40→90 mg/dl; p≥0.05). Interestingly, treatment with D. indica Page 2 of 52 bioRxiv preprint doi: https://doi.org/10.1101/804815; this version posted October 14, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 50 prevented a reduction in serum HDL levels in those hypercholesterolemic 51 model rats. Serum LDL levels were significantly lower in group-III (47→39 52 mg/dl; p≥0.05) and group-IV (57→44 mg/dl; p≥0.05) hypercholesterolemic 53 model rats after D. indica treatment. 54 Conclusion: D. indica fruit ameliorates FSG, insulin secretion, glycogen 55 synthesis, and serum lipid profile. Therefore, D. indica fruit can be a potential 56 therapeutic agent for diabetic and hyperlipidemia. 57 Keywords: D. indica fruit; Diabetes; Insulin; Lipid-Profile; Histopathology. 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 Page 3 of 52 bioRxiv preprint doi: https://doi.org/10.1101/804815; this version posted October 14, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 74 Introduction 75 Diabetes mellitus is a chronic metabolic disorder characterized by on-going 76 hyperglycemia. Insulin resistance and decreased insulin secretion are the two 77 cardinal features of type 2 diabetes mellitus (T2DM). T2DM is typically 78 diagnosed based on glucose levels, either a fasting plasma glucose (FPG) ≥ 79 7.0 or a 2-hour 75 g oral glucose tolerance test (OGTT) ≥ 11.1 mmol/L levels. 80 Pre-diabetic classifications include a fasting blood glucose (FBG) of 5.6– 81 6.9 mmol/L or a 2-hour blood glucose level of ≥7.8 and < 11.1 mmol/L [1]. 82 T2DM is often accompanied by cardiovascular disease, diabetic neuropathy, 83 nephropathy, and retinopathy. An altered lipid profile is common in T2DM 84 patients. Furthermore, reduced hepatic glycogen storage is also observed in 85 diabetes [2-4]. Advancements in the modern lifestyle over the last century 86 have contributed to a dramatic escalation in the incidence of T2DM and 87 hyperlipidemia worldwide [5, 6]. Diabetes mellitus (DM) ranks seventh among 88 the leading causes of death and ranks third when its complications are taken 89 into account [7]. One of the potential complications of T2DM is coronary heart 90 disease due to hyperlipidemia. Hyperlipidemia is a metabolic disorder 91 characterized by successive accumulation of lipids and leukocytes in the 92 arterial wall. This can contribute to many forms of diseases, especially 93 cardiovascular ones such as myocardial infarction and stroke. Moreover, 94 systemic hypercholesterolemia is associated with massive neutrophilia and 95 monocytosis [8-11]. Peripheral leukocyte amount is proportional to the level of 96 cardiovascular complications [12]. Moreover, hypercholesterolemia is 97 positively associated with systemic neutrophil as well as monocyte expansion, 98 suggesting that abnormalities in circulating lipids can influence myeloid cell Page 4 of 52 bioRxiv preprint doi: https://doi.org/10.1101/804815; this version posted October 14, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 99 expansion [13]. Thus the pathophysiological mechanism underlying 100 hypercholesterolemia is the enrichment and accumulation of systemic 101 neutrophils and monocytes which subsequently increase atherosclerosis. 102 Atherosclerosis due to hyperlipidemia (elevated levels of cholesterol, TG, 103 LDL) is the principal cause of mortality affecting people worldwide [14]. 104 According to the World Health Organization (1999), it was estimated that high 105 cholesterol level causes around one-third of all cardiovascular disease 106 worldwide and that there are 10,000,000 people with familial 107 hypercholesterolemia worldwide [15, 16]. Thus, overall prevention and 108 amelioration of T2DM and hyperlipidemia require an integrated, international 109 approach to combat the rapid increase in the number of patients in the 110 forthcoming years [5, 17]. 111 Dietary cholesterol has a direct effect on plasma levels of cholesterol [18-20]. 112 Dietary cholesterol increases serum cholesterol in all common species if high 113 enough loads are given. The extent of increase depends on the compensatory 114 mechanisms such as enhanced excretion of bile acids and neutral sterols and 115 regulation of cholesterol synthesis and absorption [21]. Lipid-lowering agents 116 have been responsible for a 30% reduction of cardiovascular diseases, 117 therefore validating the search for new therapeutic drugs to reduce 118 hyperlipidemia [22]. In addition, natural products have the potential to prevent 119 T2DM or to keep the disease under control [23-25]. The World Health 120 Organization (WHO) has also recommended evaluating the effectiveness of 121 natural products when there is a lack of safe modern drugs [26, 27]. Moreover, 122 it is believed that natural products may have fewer side effects than 123 conventional drugs. One such natural product is Dillenia indica (D. indica), Page 5 of 52 bioRxiv preprint doi: https://doi.org/10.1101/804815; this version posted October 14, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license. 124 locally known as chalta or “elephant apple”. The fruit of D. indica is a 5-12 cm 125 diameter aggregate of 15 carpels, with each carpel containing five seeds 126 embedded in an edible pulp. D. indica fruit is widely used in many indigenous 127 medicinal preparations against several diseases [28] (Supplemental Figure 1). 128 The enzyme inhibition capacity of the active constituents in D. indica has been 129 reported in several studies. For example, betulinic acid in D. indica fruits can 130 inhibit tyrosinase [29], and sterols in D. indica leaves can inhibit α-amylase 131 and α-glucosidase [30]. Nevertheless, despite its traditional claims [31], 132 limited data is available on the hypoglycemic and anti-hyperlipidemic activities 133 exerted by D. indica fruit. Here we hypothesized that D. indica fruit may 134 reduce post-prandial hyperglycemia and hyperlipidemia by suppressing 135 carbohydrate hydrolysis and lipid absorption in the gut respectively, which 136 may be beneficial for diabetic and hyperlipidemic control.
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